1887

Abstract

Apoptosis involves a cascade of caspase activation leading to the ordered dismantling of critical cell components. However, little is known about the dismantling process in non-apoptotic cell death where caspases are not involved. is a good model system to study caspase-independent cell death where experimental accessibility of non-apoptotic cell death is easier and molecular redundancy is reduced compared with other animal models. Poly(ADP-ribose) polymerase (PARP) is one of the key players in cell death. We have previously reported the role of PARP in development and the oxidative stress-induced cell death of possesses nine PARP genes and does not have a caspase gene, and thus it provides a better model system to dissect the role of PARP in caspase-independent cell death. The current study shows that non-apoptotic cell death in occurs in a programmed fashion where proteases cause mitochondrial membrane potential changes followed by plasma membrane rupture and early loss of plasma membrane integrity. Furthermore, the results suggest that calpains and cathepsin D, which are instrumental in dismantling the cell, act downstream of PARP. Thus, PARP, apoptosis inducing factor, calpains and cathepsin D are the key players in caspase-independent cell death, acting in a sequential manner.

Funding
This study was supported by the:
  • Department of Biotechnology, New Delhi (Award BT/PR9496/BRB/10/562/2007)
  • Department of Science and Technology, New Delhi (Award SR/SO/BB-03/2010)
  • Council of Scientific and Industrial Research, New Delhi
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.076620-0
2014-06-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/6/1101.html?itemId=/content/journal/micro/10.1099/mic.0.076620-0&mimeType=html&fmt=ahah

References

  1. Bidère N., Lorenzo H. K., Carmona S., Laforge M., Harper F., Dumont C., Senik A. ( 2003). Cathepsin D triggers Bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis. J Biol Chem 278:31401–31411 [View Article][PubMed]
    [Google Scholar]
  2. Cossarizza A., Salvioli S. ( 2001). Flow cytometric analysis of mitochondrial membrane potential using JC-1. Curr Protoc Cytom Chapter 9:9. 14[PubMed]
    [Google Scholar]
  3. Gautam S., Sharma A. ( 2002a). Involvement of caspase-3-like protein in rapid cell death of Xanthomonas. Mol Microbiol 44:393–401 [View Article][PubMed]
    [Google Scholar]
  4. Gautam S., Sharma A. ( 2002b). Rapid cell death in Xanthomonas campestris pv. glycines. J Gen Appl Microbiol 48:67–76 [View Article][PubMed]
    [Google Scholar]
  5. Hasnain S. E., Taneja T. K., Sah N. K., Mohan M., Pathak N., Sahdev S., Athar M., Begum R. ( 1999). In vitro cultured Spodoptera frugiperda insect cells: model for oxidative stress-induced apoptosis. J Biosci 24:13–19 [View Article]
    [Google Scholar]
  6. Hasnain S. E., Begum R., Ramaiah K. V. A., Sahdev S., Shajil E. M., Taneja T. K., Mohan M., Athar M., Sah N. K., Krishnaveni M. ( 2003). Host–pathogen interactions during apoptosis. J Biosci 28:349–358 [View Article][PubMed]
    [Google Scholar]
  7. Katoch B., Begum R. ( 2003). Biochemical basis of the high resistance to oxidative stress in Dictyostelium discoideum. J Biosci 28:581–588 [View Article][PubMed]
    [Google Scholar]
  8. Katoch B., Sebastian S., Sahdev S., Padh H., Hasnain S. E., Begum R. ( 2002). Programmed cell death and its clinical implications. Indian J Exp Biol 40:513–524[PubMed]
    [Google Scholar]
  9. Kawal A. M., Mir H., Ramniklal C. K., Rajawat J., Begum R. ( 2011). Structural and evolutionary analysis of PARPs in D. discoideum. Am J Infect Dis 7:67–74 [View Article]
    [Google Scholar]
  10. Koning A. J., Lum P. Y., Williams J. M., Wright R. ( 1993). DiOC6 staining reveals organelle structure and dynamics in living yeast cells. Cell Motil Cytoskeleton 25:111–128 [View Article][PubMed]
    [Google Scholar]
  11. Kono Y., Fridovich I. ( 1983). Isolation and characterization of the pseudocatalase of Lactobacillus plantarum. J Biol Chem 258:6015–6019[PubMed]
    [Google Scholar]
  12. Laporte C., Kosta A., Klein G., Aubry L., Lam D., Tresse E., Luciani M. F., Golstein P. ( 2007). A necrotic cell death model in a protist. Cell Death Differ 14:266–274 [View Article][PubMed]
    [Google Scholar]
  13. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J. ( 1951). Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275[PubMed]
    [Google Scholar]
  14. Madeo F., Herker E., Maldener C., Wissing S., Lächelt S., Herlan M., Fehr M., Lauber K., Sigrist S. J. & other authors ( 2002). A caspase-related protease regulates apoptosis in yeast. Mol Cell 9:911–917 [View Article][PubMed]
    [Google Scholar]
  15. Miller E. ( 2004). Apoptosis measurement by annexin v staining. Methods Mol Med 88:191–202[PubMed]
    [Google Scholar]
  16. Mir H. A., Rajawat J., Pradhan S., Begum R. ( 2007). Signaling molecules involved in the transition of growth to development of Dictyostelium discoideum. Indian J Exp Biol 45:223–236[PubMed]
    [Google Scholar]
  17. Mir H., Rajawat J., Begum R. ( 2012). Staurosporine induced cell death in D. discoideum is independent of PARP. Indian J Exp Biol 50:80–86[PubMed]
    [Google Scholar]
  18. Mohan M., Taneja T. K., Sahdev S., Mohareer K., Begum R., Athar M., Sah N. K., Hasnain S. E. ( 2003). Antioxidants prevent UV-induced apoptosis by inhibiting mitochondrial cytochrome c release and caspase activation in Spodoptera frugiperda (Sf9) cells. Cell Biol Int 27:483–490 [View Article][PubMed]
    [Google Scholar]
  19. Moubarak R. S., Yuste V. J., Artus C., Bouharrour A., Greer P. A., Menissier-de Murcia J., Susin S. A. ( 2007). Sequential activation of poly(ADP-ribose) polymerase 1, calpains, and Bax is essential in apoptosis-inducing factor-mediated programmed necrosis. Mol Cell Biol 27:4844–4862 [View Article][PubMed]
    [Google Scholar]
  20. Olie R. A., Durrieu F., Cornillon S., Loughran G., Gross J., Earnshaw W. C., Golstein P. ( 1998). Apparent caspase independence of programmed cell death in Dictyostelium. Curr Biol 8:955–958 [View Article][PubMed]
    [Google Scholar]
  21. Polster B. M., Fiskum G. ( 2004). Mitochondrial mechanisms of neural cell apoptosis. J Neurochem 90:1281–1289 [View Article][PubMed]
    [Google Scholar]
  22. Rajawat J., Vohra I., Mir H. A., Gohel D., Begum R. ( 2007). Effect of oxidative stress and involvement of poly(ADP-ribose) polymerase (PARP) in Dictyostelium discoideum development. FEBS J 274:5611–5618 [View Article][PubMed]
    [Google Scholar]
  23. Rajawat J., Mir H., Begum R. ( 2011). Differential role of poly(ADP-ribose) polymerase in D. discoideum growth and development. BMC Dev Biol 11:14 [View Article][PubMed]
    [Google Scholar]
  24. Rajawat J., Mir H., Alex T., Bakshi S., Begum R. ( 2014). Involvement of poly(ADP-ribose) polymerase in paraptotic cell death of D. discoideum. Apoptosis 19:90–101 [View Article][PubMed]
    [Google Scholar]
  25. Roisin-Bouffay C., Luciani M. F., Klein G., Levraud J. P., Adam M., Golstein P. ( 2004). Developmental cell death in Dictyostelium does not require paracaspase. J Biol Chem 279:11489–11494 [View Article][PubMed]
    [Google Scholar]
  26. Sah N. K., Taneja T. K., Pathak N., Begum R., Athar M., Hasnain S. E. ( 1999). The baculovirus antiapoptotic p35 gene also functions via an oxidant-dependent pathway. Proc Natl Acad Sci U S A 96:4838–4843 [View Article][PubMed]
    [Google Scholar]
  27. Sanges D., Comitato A., Tammaro R., Marigo V. ( 2006). Apoptosis in retinal degeneration involves cross-talk between apoptosis-inducing factor (AIF) and caspase-12 and is blocked by calpain inhibitors. Proc Natl Acad Sci U S A 103:17366–17371 [View Article][PubMed]
    [Google Scholar]
  28. Sanvicens N., Gómez-Vicente V., Masip I., Messeguer A., Cotter T. G. ( 2004). Oxidative stress-induced apoptosis in retinal photoreceptor cells is mediated by calpains and caspases and blocked by the oxygen radical scavenger CR-6. J Biol Chem 279:39268–39278 [View Article][PubMed]
    [Google Scholar]
  29. Saraste A., Pulkki K. ( 2000). Morphologic and biochemical hallmarks of apoptosis. Cardiovasc Res 45:528–537 [View Article][PubMed]
    [Google Scholar]
  30. Sperandio S., de Belle I., Bredesen D. E. ( 2000). An alternative, nonapoptotic form of programmed cell death. Proc Natl Acad Sci U S A 97:14376–14381 [View Article][PubMed]
    [Google Scholar]
  31. Turk B., Stoka V. ( 2007). Protease signalling in cell death: caspases versus cysteine cathepsins. FEBS Lett 581:2761–2767 [View Article][PubMed]
    [Google Scholar]
  32. Watts D. J., Ashworth J. M. ( 1970). Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem J 119:171–174[PubMed]
    [Google Scholar]
  33. Wood D. E., Newcomb E. W. ( 1999). Caspase-dependent activation of calpain during drug-induced apoptosis. J Biol Chem 274:8309–8315 [View Article][PubMed]
    [Google Scholar]
  34. Wood D. E., Thomas A., Devi L. A., Berman Y., Beavis R. C., Reed J. C., Newcomb E. W. ( 1998). Bax cleavage is mediated by calpain during drug-induced apoptosis. Oncogene 17:1069–1078 [View Article][PubMed]
    [Google Scholar]
  35. Zong W. X., Thompson C. B. ( 2006). Necrotic death as a cell fate. Genes Dev 20:1–15 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.076620-0
Loading
/content/journal/micro/10.1099/mic.0.076620-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error